Interleukin-27 Is a Potential Rescue Therapy for Acute Severe Colitis Through Interleukin-10-Dependent, T-Cell-Independent Attenuation of Colonic Mucosal Innate Immune Responses

Inflammatory Bowel Diseases

Volumn 23, Issue 11, 2017, Pages 1983-1995

  McLean, Mairi H ^a,b   Andrews, Caroline ^a   Hanson, Miranda L ^a   Baseler, Walter A ^a   Anver, Miriam R ^c   Senkevitch, Emilee ^a   Staniszewska, Aleksandra K ^a,b   Smith, Christopher ^a,b   Davies, Luke C ^a   Hixon, Julie ^a   Li, Wenqeng ^a   Shen, Wei ^a   Steidler, Lothar ^d   Durum, Scott K ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d INTREXON CORPORATION   (United States)

Author keywords

colitis; cytokine; inflammatory bowel disease; interleukin 27

Indexed keywords

ALPHA CHEMOKINE; INTERLEUKIN 10; INTERLEUKIN 27; STAT1 PROTEIN; TRINITROBENZENESULFONIC ACID;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; COLITIS; COLON EPITHELIUM; COLON MUCOSA; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; EPITHELIUM CELL; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; INNATE IMMUNITY; LACTOCOCCUS LACTIS; MALE; MOUSE; MUCOSAL IMMUNITY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TREATMENT RESPONSE; ANIMAL; CHEMICALLY INDUCED; COLON; DISEASE MODEL; DRUG EFFECT; IMMUNOLOGY; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ACUTE DISEASE; ANIMALS; COLITIS; COLON; DISEASE MODELS, ANIMAL; IMMUNITY, INNATE; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-10; INTERLEUKIN-27; INTESTINAL MUCOSA; MALE; MICE; MICE, KNOCKOUT; T-LYMPHOCYTES; TRINITROBENZENESULFONIC ACID;

EID: 85040722980     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000001274     Document Type: Article

References (43)

1. Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annu Rev Immunol. 2010;28:573-621.
2. Molodecky NA, Soon IS, Rabi DM, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142:46-54.
3. Ford AC, Sandborn WJ, Khan KJ, et al. Efficacy of biological therapies in inflammatory bowel disease: systematic review and meta-analysis. Am J Gastroenterol. 2011;106:644-659.
4. Danese S, Colombel JF, Peyrin-Biroulet L, et al. Review article: the role of anti-TNF in the management of ulcerative colitis-past, present and future. Aliment Pharmacol Ther. 2013;37:855-866.
5. Fornaro R, Caratto M, Barbruni G, et al. Surgical and medical treatment in patients with acute severe ulcerative colitis. J Dig Dis. 2015;16:558-567.
6. Macken L, Blaker PA. Management of acute severe ulcerative colitis (NICE CG 166). Clin Med (Lond).s 2015;15:473-476.
7. \Oresland T, Bemelman WA, Sampietro GM, et al; European Crohn's and Colitis Organisation (ECCO). European evidence based consensus on surgery for ulcerative colitis. J Crohns Colitis. 2015;9:4-25.
8. Carlsson E, Bosaeus I, Nordgren S. What concerns subjects with inflammatory bowel disease and an ileostomy? Scand J Gastroenterol. 2003;38: 978-984.
9. Knowles SR, Cook SI, Tribbick D. Relationship between health status, illness perceptions, coping strategies and psychological morbidity: a preliminary study with IBD stoma patients. J Crohns Colitis. 2013;7:e471-e478.
10. Spinelli A, Carvello M, D'Hoore A, et al. Psychological perspectives of inflammatory bowel disease patients undergoing surgery: rightful concerns and preconceptions. Curr Drug Targets. 2014;15:1074-1078.
11. Hanson ML, Hixon JA, Li W, et al. Oral delivery of IL-27 recombinant bacteria attenuates immune colitis in mice. Gastroenterology. 2014;146: 210-221.
12. Stumhofer JS, Hunter CA. Advances in understanding the antiinflammatory properties of IL-27. Immunol Lett. 2008;117:123-130.
13. Wojno ED, Hunter CA. New directions in the basic and translational biology of interleukin-27. Trends Immunol. 2012;33:91-97.
14. Wynick C, Petes C, Gee K. Interleukin-27 mediates inflammation during chronic disease. J Interferon Cytokine Res. 2014;34:741-749.
15. Pflanz S, Timans JC, Cheung J, et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4+ T cells. Immunity. 2002;16:779-790.
16. Li JP, Wu H, Xing W, et al. Interleukin-27 as a negative regulator of human neutrophil function. Scand J Immunol. 2010;72:284-292.
17. Iyer SS, Ghaffari AA, Cheng G. Lipopolysaccharide-mediated IL-10 transcriptional regulation requires sequential induction of type I IFNs and IL-27 in macrophages. J Immunol. 2010;185:6599-6607.
18. Shimizu M, Ogura K, Mizoguchi I, et al. IL-27 promotes nitric oxide production induced by LPS through STAT1, NF-kB and MAPKs. Immunobiology. 2013;218:628-634.
19. Rinchai D, Khaenam P, Kewcharoenwong C, et al. Production of interleukin-27 by human neutrophils regulates their function during bacterial infection. Eur J Immunol. 2012;42:3280-3290.
20. Wang S, Miyazaki Y, Shinozaki Y, et al. Augmentation of antigenpresenting and Th1-promoting functions of dendritic cells by WSX-1 (IL-27R) deficiency. J Immunol. 2007;179:6421-6428.
21. Mascanfroni ID, Yeste A, Vieira SM, et al. IL-27 acts on DCs to suppress the T cell response and autoimmunity by inducing expression of the immunoregulatory molecule CD39. Nat Immunol. 2013;14:1054-1063.
22. Morandi F, Di Carlo E, Ferrone S, et al. IL-27 in human secondary lymphoid organs attracts myeloid dendritic cells and impairs HLA class I-restricted antigen presentation. J Immunol. 2014;192:2634-2642.
23. Xu F, Liu Q, Lin S, et al. IL-27 is elevated in acute lung injury and mediates inflammation. J Clin Immunol. 2013;33:1257-1268.
24. Cao J, Xu F, Lin S, et al. IL-27 controls sepsis-induced impairment of lung antibacterial host defence. Thorax. 2014;69:926-937.
25. Diegelmann J, Olszak T, Göke B, et al. A novel role for interleukin-27 (IL-27) as mediator of intestinal epithelial barrier protection mediated via differential signal transducer and activator of transcription (STAT) protein signaling and induction of antibacterial and anti-inflammatory proteins. J Biol Chem. 2012;287:286-298.
26. Wirtz S, Tubbe I, Galle PR, et al. Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27. J Exp Med. 2006; 203:1875-1881.
27. De Filippo K, Dudeck A, Hasenberg M, et al. Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood. 2013;121:4930-4937.
28. Scheiffele F, Fuss IJ. Induction of TNBS colitis in mice. Curr Protoc Immunol. 2002;Chapter 15:Unit 15.19.
29. Awasthi A, Carrier Y, Peron JP, et al. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol. 2007;8:1380-1389.
30. Hunter CA, Kastelein R. Interleukin-27: balancing protective and pathological immunity. Immunity. 2012;37:960-969.
31. Apetoh L, Quintana FJ, Pot C, et al. The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol. 2010;11:854-861.
32. Koltsova EK, Kim G, Lloyd KM, et al. Interleukin-27 receptor limits atherosclerosis in Ldlr-/-mice. Circ Res. 2012;111:1274-1285.
33. Nauseef WM, Borregaard N. Neutrophils at work. Nat Immunol. 2014;15: 602-611.
34. Guzzo C, Che Mat NF, Gee K. Interleukin-27 induces a STAT1/3 and NF-kappaB dependent proinflammatory cytokine profile in human monocytes. J Biol Chem. 2010;285:24404-24411.
35. Guzzo C, Ayer A, Basta S, et al. IL-27 enhances LPS-induced proinflammatory cytokine production via upregulation of TLR4 expression and signaling in human monocytes. J Immunol. 2012;188: 864-873.
36. Visperas A, Do JS, Bulek K, et al. IL-27, targeting antigen-presenting cells, promotes Th17 differentiation and colitis in mice. Mucosal Immunol. 2014;7:625-633.
37. Pot C, Apetoh L, Awasti A, et al. Induction of regulatory Tr1 cells and inhibition of TH17 cells by IL-27. Semin Immunol. 2011;23: 438-445.
38. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13:159-175.
39. Ohtsuka Y, Lee J, Stamm DS, et al. MIP-2 secreted by epithelial cells increases neutrophil and lymphocyte recruitment in the mouse intestine. Gut. 2001;49:526-533.
40. Ohtsuka Y, Sanderson IR. Dextran sulfate sodium-induced inflammation is enhanced by intestinal epithelial cell chemokine expression in mice. Pediatr Res. 2003;53:143-147.
41. Bermúdez-Humarán LG, Kharrat P, Chatel JM, et al. Lactococci and lactobacilli as mucosal delivery vectors for therapeutic proteins and DNA vaccines. Microb Cell Fact. 2011;10(suppl 1):S4.
42. Steidler L, Hans W, Schotte L, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science. 2000;289: 1352-1355.
43. Steidler L, Rottiers P, Coulie B. Actobiotics as a novel method for cytokine delivery. Ann N Y Acad Sci. 2009;1182:135-145.